INTRODUCTION
Copepods are the most common and widely distributed group of small aquatic crustaceans. Copepods have an important role in the food web, linking primary producers and higher trophic levels, in aquatic systems (Richmond et al., Reference Richmond, Wethey and Woodin2007). This link is essential for the optimal functioning of an ecosystem but at the same time it also implies a vulnerable point in a changing environment. Global changes in weather patterns driven by extreme events (floods and/or droughts) may have severe repercussion in reproduction, migration and abundances of copepods and thus in multiple species of aquatic food webs (Roff, Reference Roff1992; Richmond et al., Reference Richmond, Wethey and Woodin2007). Especially in a changing environment like an estuary, it is essential to understand the natural degree of variation of copepod communities.
In general, copepods dominate mesozooplankton communities (Kršinić & Grbec, Reference Kršinić and Grbec2002; Cornils et al., Reference Cornils, Schnack-Schiel, Al-Najjar, Badran, Rasheed, Manasreh and Richter2007). Among copepods, cyclopoids usually dominate the summer and autumn assemblages, whereas calanoids are predominant in winter and spring (Calbet et al., Reference Calbet, Garrido, Saiz, Alcaraz and Duarte2001; Kršinić & Grbec, Reference Kršinić and Grbec2002; Cornils et al., Reference Cornils, Schnack-Schiel, Al-Najjar, Badran, Rasheed, Manasreh and Richter2007). Indeed, copepod nauplii are most abundant in spring, followed by calanoid and cyclopoid copepodites, respectively. Whereas harpacticoids represent a less abundant fraction in copepod community (Calbet et al., Reference Calbet, Garrido, Saiz, Alcaraz and Duarte2001; Kršinić & Grbec, Reference Kršinić and Grbec2002; Cornils et al., Reference Cornils, Schnack-Schiel, Al-Najjar, Badran, Rasheed, Manasreh and Richter2007), this order constitutes a diverse group and the second most abundant with respect to meiofauna taxon (Huys & Boxshall, Reference Huys and Boxshall1991; Suárez-Morales et al., Reference Suárez-Morales, De Troch and Fiers2006). They are well adapted to different environments resulting in a wide range of morphological diversity in benthic and planktonic organisms (Huys & Boxshall, Reference Huys and Boxshall1991). Harpacticoids are an important food source for higher trophic levels, whose reduction may cause profound impacts in many other estuarine species, such as fish communities, as well as in species of other habitats that spend their earlier life stages in estuaries. Although several studies demonstrated seasonal variations of these communities due to abiotic and biotic factors (e.g. temperature, salinity, food availability and turbidity), some species of copepods showed no clear seasonal trends (Calbet et al., Reference Calbet, Garrido, Saiz, Alcaraz and Duarte2001; Kršinić & Grbec, Reference Kršinić and Grbec2002; Uriarte & Villate, Reference Uriarte and Villate2004, Reference Uriarte and Villate2005; Cornils et al., Reference Cornils, Schnack-Schiel, Al-Najjar, Badran, Rasheed, Manasreh and Richter2007).
Despite several studies being based on the composition of marine harpacticoid fauna (Lang, Reference Lang1948, Reference Lang1965a; Huys et al., Reference Huys, Gee, Moore and Hammond1996), they were restricted to a limited number of habitats or specific areas such as the Gulf of Mexico and other tropical areas (Fleeger & Clark, Reference Fleeger and Clark1979; Rutledge & Fleeger, Reference Rutledge and Fleeger1993; Fiers, Reference Fiers1995, Reference Fiers1996; Suárez-Morales et al., Reference Suárez-Morales, Reid, Gasca, Llorente-Bousquets, Aldrete and Soriano2000, Reference Suárez-Morales, De Troch and Fiers2006). In Portugal, few works have been carried out with a focus on harpacticoid copepods' ecology and taxonomy (Galhano, Reference Galhano1968; Noodt & Galhano, Reference Noodt and Galhano1969; Morgado, Reference Morgado1997).
The objective of the present study is to document the natural variation of harpacticoid copepods in a typical European estuary. The Mondego estuary (shallow temperate mesotidal estuary) is located along the western coast of Portugal, a warm temperate region, constituting an important system to support human and industrial activities. Figueira da Foz city and its tourism activities cause seasonal pressure on the system (Marques et al., Reference Marques, Graça, Pardal, Pardal, Marques and Graça2002). Similarly to other estuaries, Mondego estuary receives large amounts of nutrients from agriculture fields, contributing to the developing of eutrophication events (Pardal et al., Reference Pardal, Marques, Metelo, Lillebø and Flindt2000). So far, the Mondego estuary is documented in terms of the effects of eutrophication on benthic populations' structure and distribution (Pardal et al., Reference Pardal, Marques, Metelo, Lillebø and Flindt2000; Cardoso et al., Reference Cardoso, Pardal, Lillebø, Ferreira, Raffaelli and Marques2004; Verdelhos et al., Reference Verdelhos, Neto, Marques and Pardal2005), and on zooplankton distribution and dynamics (Azeiteiro et al., Reference Azeiteiro, Marques and Ré1999; Gonçalves et al., Reference Gonçalves, Ribeiro and Soares2003; Marques et al., Reference Marques, Azeiteiro, Marques, Neto and Pardal2006, Reference Marques, Pardal, Pereira, Gonçalves, Marques and Azeiteiro2007, Reference Marques, Azeiteiro, Leandro, Queiroga, Primo, Viegas and Pardal2008; Primo et al., Reference Primo, Azeiteiro, Marques, Martinho and Pardal2009). The first results of the implementation of the management plan to promote the recovery of Mondego estuary originated a reduction in the dissolved nutrients and green macroalgal blooms with the recovery of the seagrass beds (Verdelhos et al., Reference Verdelhos, Neto, Marques and Pardal2005; Dolbeth et al., Reference Dolbeth, Cardoso, Ferreira, Verdelhos, Raffaelli and Pardal2007; Cardoso et al., Reference Cardoso, Raffaeli, Lillebø, Verdelhos and Pardal2008). Consequently, a higher biomass and growth production has been observed in the whole intertidal area. However, severe effects on macrobenthic assemblages due to naturally induced stressors started to be noticeable, with drastic socio-economic impacts related with high mortality of fish and the reduction of some economically important species of bivalves (e.g. Scrobicularia plana and Cerastoderma edule). Despite the extensive literature on the Mondego benthic and pelagic ecology, the species composition and distribution of harpacticoids in the two arms of the Mondego estuary remain unknown.
This paper presents the first study of Harpacticoida community and compares the distribution of harpacticoid species in both arms of the Mondego estuary in relation to spatial and seasonal environmental variations.
MATERIALS AND METHODS
Study site
The Mondego estuary, located on the western coast of Portugal (40°08′N 8°50′W) consists of two arms—north and south—with different hydrological characteristics, separated by Murraceira Island (Figure 1). The northern arm with a lower residence time (<1 day), is deeper (4–8 m at high tide, tidal range 1–3 m) and forms the main navigation channel, serving the Figueira da Foz harbour and connects directly to the Mondego River. The southern arm is more shallow (2–4 m deep, at high tide, tidal range about 1–3 m), with higher residence times (2–8 days). This channel is largely silted up, especially in the upstream areas, forcing most of the freshwater discharge to flow out through the northern arm (Pardal et al., Reference Pardal, Marques, Metelo, Lillebø and Flindt2000; Cardoso et al., Reference Cardoso, Pardal, Lillebø, Ferreira, Raffaelli and Marques2004). The water circulation in the southern arm is predominantly due to the tidal cycle and to a relatively small freshwater input of a tributary, the Pranto River, which is artificially controlled by a sluice, according to the water needs on rice fields (Marques et al., Reference Marques, Graça, Pardal, Pardal, Marques and Graça2002). As for many other regions, this system suffers from direct and indirect human effects related to intensive agriculture, harbour facilities and economic growth at the regional scale. Since the late 1980s, the south arm shows symptoms of eutrophication as a result of anthropogenic activities. The system is gradually recovering after the implementation of mitigation measures in 1998 which enhanced environmental quality (Cardoso et al., Reference Cardoso, Brandão, Pardal, Raffaelli and Marques2005; Dolbeth et al., Reference Dolbeth, Cardoso, Ferreira, Verdelhos, Raffaelli and Pardal2007). Until the beginning of 2006 this sub-system was almost silted up in the upstream areas. Since then, several works have been carried out in order to establish the connection between the two arms (Dolbeth et al., Reference Dolbeth, Cardoso, Ferreira, Verdelhos, Raffaelli and Pardal2007).
Map of the Mondego estuary, located on the western coast of Portugal. Sampling stations are indicated: M, mouth station; N1 and N2, northern arm stations; S1 and S2, southern arm stations.
Sampling
Harpacticoid samples were collected monthly from February 2005 to January 2007 at five stations of Mondego estuary situated in both arms of the estuary in order to cover a maximum and representative area of the system (M, mouth of the estuary; N1 and N2, northern arm of the estuary; S1 and S2, southern arm of the estuary, Figure 1). Sampling was carried out during high tide, with a 63-µm mesh Bongo net, with 0.30 m diameter and the organisms were fixed in 4% buffered formaldehyde. Environmental parameters (salinity, temperature, dissolved oxygen concentration, pH and transparency) were measured in situ. In each sampling station subsurface water samples were collected for nutrient concentration analysis (Si, PO4, NO2, NO3, NH4), determination of chlorophyll-a (Chl-a) and total suspended solids (TSS). Monthly precipitation values were measured at the Soure 13 F/01G station and acquired from INAG—Portuguese Water Institute (http://snirh.inag.pt).
Laboratory procedures
Standard methods were followed to determine nutrient concentrations (Limnologisk Metodik, 1992—for ammonia and phosphate; Strickland & Parsons, Reference Strickland and Parsons1972—for nitrate and nitrite). Chlorophyll-a concentration was determined by filtering 500–1000 ml of water through GF/C filters, which were then treated with acetone (90%) to extract the Chl-a measured at 630, 647, 665 and 750 nm (Parsons et al., Reference Parsons, Maita, Lally, Parsons, Maita and Lally1985). Dry weight (TSS) was estimated by filtering 500–1000 ml water through Whatman GF/C filters, tarred and dried at 60°C for 72 hours and combustion at 450°C for 8 hours (APHA, 1995).
From each sample, all harpacticoid copepods were counted, picked out and stored in ethanol. Glycerine slides were prepared with in toto adults. Harpacticoid copepods were identified to the lowest taxonomic level using the identification keys and reference books by Lang (Reference Lang1948, Reference Lang1965a), Huys et al. (Reference Huys, Gee, Moore and Hammond1996), Boxshall & Halsey (Reference Boxshall and Halsey2004) and original genus and species descriptions. The nomenclature of families and genera in the checklist followed Bodin (Reference Bodin1997) and Wells (Reference Wells2007).
Data analysis
A cluster analysis using the PRIMER statistical package (Clarke & Warwick, Reference Clarke and Warwick2001) was performed in order to group harpacticoid species with similar distribution and occurrence. The Bray–Curtis similarity index was followed to calculate distance between groups, using complete linkage as clustering method. A redundancy data analysis (RDA) was carried out, using the CANOCO v. 4.5 package (ter Braak & Smilauer, Reference ter Braak and Smilauer1998), on both matrices where columns were the taxonomic groups and environmental parameters, respectively, and rows of the seasonal data, which were estimated by averaging the monthly values from each station, to identify the relationship between species distribution and environmental factors. Prior to these analyses, Harpactioida densities were square-root transformed.
A spatial and seasonal variation analysis was performed for the five sampling stations in order to investigate and compare the seasonal variability of community structure. The seasonal periods defined are: winter—December, January and February; spring—March, April and May; summer—June, July and August; autumn—September, October and November. Each season account with two average months (e.g. Spring 05 and Spring 06) whereas the winter season reports to three average months (W05; W06 and W07).
RESULTS AND DISCUSSION
Environmental parameters
Annual precipitation average from 1961 to 1990 was 1016 mm (http://snirh.inag.pt). Figure 2 shows the normal climate for central Portugal (IM—Portuguese Weather Institute, http://web.meteo.pt). The study period presented different hydrological years: 2005–2006 more arid, and 2006–2007 a period with periodic wet months (Figure 2). Nevertheless, precipitation was lower (2005–2006: 855.9 mm and 2006–2007: 866.5 mm) than the normal precipitation average (1016 mm). In general, nitrate and silica concentrations showed a reduction in their values from winter to summer, but phosphate concentrations showed an irregular seasonal pattern, with higher values being associated with the upstream stations (Table 1). In the upstream stations an increase of Chl-a concentration was observed, especially in spring and summer at the north arm station, and for all seasons, except in spring, in the south arm station (e.g. Station N2: 10.48 in spring and 11.11 mg m−3 in summer; Station S2: 18.97 in winter and 17.33 in summer; and 14.69 mg m−3 in autumn). Total suspended solids (TSS) showed a decrease from the upstream towards the downstream stations in the northern arm, except in spring/summer, where the highest values were obtained at Station N1 (25.06 and 26.06 mg l−1). In the southern arm, a decrease from upstream to downstream stations was also found. Turbidity values revealed a rise from downstream to upstream stations in both arms (Table 1). In general, the water temperature was higher in spring and summer and lower in autumn and winter, following a typical pattern for temperate latitudes. The values ranged from 10.46°C to 24.26°C, reaching minimum and maximum values during winter and summer at Station S2, respectively. The Stations S1 and M had the highest salinities, ranging from 15.32 psu (in winter at Station M) to 31.56 psu (in summer at Station S1). In general, Station N2 showed the lowest values of salinity (winter 0.93, spring 6.75, summer 10.76 and autumn 1.20 psu).
Monthly precipitation (mm) in Mondego estuary during the study period (2005–2006 and 2006–2007). Grey filled circles represent a monthly average of 1961 to 1990 (http://snirh.inag.pt).
Physical and chemical parameters (Si, silica; PO4, phosphates; NO2, nitrites; NO3, nitrates; NH4, ammonia; Chl-a, chlorophyll-a; TSS, total suspended solids; O2, dissolved oxygen; Temp, temperature; Sal, salinity; Turb, turbidity) at each sampling station ((M, mouth station; N1 and N2, northern arm stations, S1 and S2, southern arm stations), during seasonal cycles (W, winter (December, January and February); Sp, spring (March, April and May); S, summer (June, July and August); A, autumn (September, October and November)). Average values of two sampling actions in two years.
Harpacticoid copepod composition
The harpacticoid copepods belonged to 14 harpacticoid families in which 13 species were identified plus six specimens that were identified to the genus level (namely Canuella, Microsetella, Ectinosoma, Mesochra, Harpacticus and Parapseudoleptomesochra). Table 2 gives a taxonomic overview of the species identified. The families Ectinosomatidae and Ameiridae were the most diverse followed by the other families represented by only one species/genus. Euterpina acutifrons (family Euterpinidae) and Paronychocamptus nanus (family Laophontidae) were widely distributed in the estuary. In spite of the initial aim of our sampling campaign to collect planktonic copepods, several harpacticoid copepods that were collected in the water column are benthic forms. A checklist of the harpacticoid copepods identified in Mondego estuary is provided below. Scientific names are employed for each taxonomic group to the lowest taxonomic level possible in order to give the most complete nomenclature information.
List of abbreviations and individual abundance (%) of Harpacticoid species (subclass Copepoda Milne-Edwards, 1840; order Harpacticoida Sars, 1903) used in data analyses.
Subclass copepoda Milne-Edwards, 1840
This species list is comparable to the one reported by Morgado (Reference Morgado1997) from the estuary of Ria de Aveiro, located 50 km north of the Mondego estuary. In spite of the fact that Morgado (Reference Morgado1997) used a 125-µm sieve, several harpacticoid species were found in common, namely adults and copepodites of Euterpina acutifrons, Microsetella sp., Ectinosoma sp., Harpacticus obscurus, Tachidius discipes, Metis cfr. ignea, Mesochra sp. and Paronychocamptus nanus. Morgado (Reference Morgado1997) found T. discipes and E. acutifrons to be the two most abundant species.
A cluster analysis (Figure 3) showed the affinity between species/genus identified in the five stations of the Mondego estuary. Group I is composed of the most related species, Metis cfr. ignea and Tachidius discipes, due to their high distribution in Station S2 during the winter of 2005. The high abundance of T. discipes in Station S2 is related to the highest TSS value that was recorded in this southern arm station, in comparison with the other sampling sites (see Table 1). Group II is the most representative, comprising the species with the highest densities and highest frequency of occurrence in the estuary. The distribution of this group of harpacticoid species may be due to their high level of adaptability to environmental variance. Species of Groups II, III, V, VI and VII presented a high affinity due to high densities recorded in autumn 2005, spring 2006, spring 2005/2006, winter 2005 and 2007 and autumn 2006, respectively. Group IV comprised rare species, occurring at one or two of the sampling stations, in a specific season: Canuella sp., Phyllognathopus viguieri, Microsetella norvegica (juveniles) and Macrosetella gracilis (juveniles) occurred mostly in winter in the northern arm stations; Microsetella norvegica (juveniles) and Ectinosoma melaniceps appeared in summer in the south and north arm stations, respectively; Leptocaris brevicornis appeared in autumn in the southern arm of the estuary. The species of this group still showed no affinity among them nor between the species of the other groups.
Cladogram (cluster analysis) grouping harpacticoid species–genus groups based on their distribution in different stations. The seven species–groups of Harpacticoida are indicated by roman numbers.
A RDA analysis (Figure 4) shows the occurrence of harpacticoid species in relation to the environmental variables (NO3, PO4, NH4, Si, NO2, pH, turbidity, Chl-a, temperature, O2, salinity and TSS). The eigenvalues for axis 1 (0.361) explained 91.6% of the cumulative variance in the species data relative to the total variation explained by the environmental variables. Adults and juveniles of Microsetella sp., and Euterpina acutifrons are associated with maximal concentrations of NO2 and TSS, while Canuella sp., Praeleptomesochra phreatica, Nannopus palustris, Macrosetella gracilis and Parapseudoleptomesochra sp. correlate with higher amounts of Si and PO4. Similarly, Pesce (Reference Pesce1981) reported P. phreatica from freshwater samples from North Africa (Morocco). Ectinosoma melaniceps, Tachidius discipes (including juveniles), Metis cfr. ignea, Harpacticus obscurus and Mesochra sp. grouped in the lower part of the plot, associated with high salinities and O2 concentrations. The harpacticoids—Paronychocamptus nanus (adults and juveniles), Leptocaris brevicornis and Paraleptastacus spinicauda—were found in the upper part of the plot, associated with high concentrations of NH4.
Results of RDA analysis. Relationships between harpacticoid species distribution and environmental variables in Mondego estuary from February 2005 to January 2007.
A seasonal distribution of harpacticoid species (adults and juveniles) was performed to compare species' densities in the sampling stations and to define the most representative species in each sampling station and season. The northern arm of the estuary especially was characterized by a high density of harpacticoids during the whole year, with the highest abundances in Station N2 (Figure 5).
Average harpacticoid copepod densities (±standard error) in the different seasons and different stations: M, mouth station; N1 and N2, northern arm stations; S1 and S2, southern arm stations.
More harpacticoids (copepodites and adults) were found in the northern and southern arms (Figures 6 & 7). Copepodites and adults of Euterpina acutifrons and Paronychocampus nanus were dominant depending on the season. In general, P. nanus dominated in winter (W) and spring (Sp) seasons, except in spring at Stations M, N1 and S1, which were dominated by E. acutifrons. Paraleptastacus cfr. spinicauda showed an occurrence of 5–10% at all stations, except for Station M, where no distribution was observed. Microstella sp. showed a similar percentage of occurrences in spring/summer at Stations M and S1 and in winter/summer at Station S2. In general, this genus appears in the five stations sampled in the estuary during spring/summer, but showed lower abundances at Stations N1 and N2. These results are reinforced in Figure 8, which compares the seasonal and spatial occurrence of the two most abundant species in the estuary (E. acutifrons and P. nanus) with neritic–oceanic species (Microsetella sp. and Macrosetella gracilis). Microsetella sp. and Macrosetella gracilis represented a lower abundance. Still, the last one appears more regularly in the southern arm than in the northern arm, with a maximum density of Microsetella sp. in the five sampling stations.
Relative abundance (%) of harpacticoid species/genera in each sampling station. (A) Mouth station; (B) Station N1; (C) Station N2; (D) Station S1; (E) Station S2, during seasonal period: W, winter; Sp, spring; S, summer; A, autumn.
Seasonal pattern of the composition of harpacticoid copepods community in (A) northern and (B) southern arms of Mondego estuary.
Seasonal cycle of the most abundant harpacticoid copepods species (Euterpina acutifrons and Paronychocamptus nanus) versus neritic–oceanic species (Macrosetella gracilis and Microsetella norvegica). February 2005–January 2007.
Harpacticoid copepods are known to occur in the sediment (benthic) and on aquatic plants (epiphytic). However, the presence of benthic harpacticoids in plankton samples can be due to suspension processes and also to active migration (Walters & Bell, Reference Walters and Bell1994; Villate, Reference Villate1997; Uriarte & Villate, Reference Uriarte and Villate2005). The deepness of the sampling sites is not below 2 m, achieving 8 m in the north arm. In addition, the sampling always occurred at high tide, when the tidal range was at maximum, as stated above.
Uriarte & Villate (Reference Uriarte and Villate2004, 2005) studied the abundance and spatial distribution of copepods species and other zooplankton species in the polluted estuary of Bilbao and the unperturbed Urdaibai estuary of the Basque coast (Bay of Biscay). The authors stated that mainly environmental factors affect the distribution and structure of copepods and other zooplankton communities. In addition, copepods showed a low tolerance to hypoxia as they are present in higher abundance in unpolluted areas or in areas with moderate pollution (Siokou-Fragou & Papathanassiou, Reference Siokou-Frangou and Papathanassiou1991; Roman et al., Reference Roman, Gauzens, Rhinenart and White1993). In general, inter-estuarine comparisons showed that copepod abundances were higher in the Urdaibai estuary at high salinities, with E. acutrifrons being abundant at all salinities and meiobenthic harpacticoids only at the stations with salinities of 31 and 34 psu. Some copepod species show clear seasonal patterns of dominance or differences between estuaries or stations. For instance, Paracalanus parvus and Acartia clausi had high abundance in the Urdaibai and Bilbao estuaries, respectively, and were the copepod species with the highest seasonal alternation in the dominance in each estuary and between estuaries' differences. Oncaea media and Temora stylifera still dominated in summer with no significant differences between estuaries or salinity stations, while Pseudocalanus elongates in full please showed higher abundance in winter/spring and in sites with low salinities. As reported by other authors, harpacticoids were found in small densities, showing no clear seasonal trends and differing between estuaries rather than between salinity stations (Uriarte & Villate, Reference Uriarte and Villate2005). Euterpina acutifrons was much more abundant in the unpolluted estuary of Urdaibai presenting a uniform distribution in both estuaries. This species revealed a high adaptation to environmental factors and also to pollution gradients.
Kršinić & Grbec (Reference Kršinić and Grbec2002) studied the distribution of small zooplankton at two stations in the Otranto Strait (eastern Mediterranean), with a plankton net of 53-µm mesh size. Although harpacticoids were the group with the lowest density, they dominated in spring (May 1990). However, the authors did not observe, unlike other groups, any seasonal variation of small copepod fauna in the study area. Copepodites and adults of Microsetella sp. and Macrosetella sp. were identified, whereas other taxa were rare or absent. Similarly, our results show higher abundance in spring, for all stations, although, the species showed no significant variance in the sampling period. Accordingly, Microsetella sp. was one of the species found with the highest abundance in Mondego estuary. In the northern Gulf of Aqaba (Red Sea), Cornils et al. (Reference Cornils, Schnack-Schiel, Al-Najjar, Badran, Rasheed, Manasreh and Richter2007) studied the seasonal cycle of mesozooplankton using a net of 200-µm mesh size and found harpacticoids occurring in their lowest numbers (less than 1%) with the highest densities of copepods in spring and in autumn. Other studies have been carried out by Calbet et al. (Reference Calbet, Garrido, Saiz, Alcaraz and Duarte2001) in the Bay of Blanes (north-west Mediterranean) within an annual cycle. Sampling included an oblique tow using a 200-µm net and vertical tows using a 53-µm net. Despite copepods' groups found by other authors, Calbet et al. (Reference Calbet, Garrido, Saiz, Alcaraz and Duarte2001) concluded cyclopoids copepods dominated the summer and autumn communities while calanoid copepods were predominant in winter and spring, with no reference to harpacticoids found.
So far, there are few reports on harpacticoid copepod species in Portuguese estuarine systems. The harpacticoid families identified in the present study are benthic forms which may live in and on the fine and upper sandy sediments, which explains their presence in zooplankton samplings. The low deepness of the study sites and tidal influence in eroding the sediment bed and resuspension mechanisms creates new sedimentation areas colonized by harpacticoid copepods. Morgado (Reference Morgado1997) observed a comparable composition and distribution pattern of harpacticoid species, collected with a 125-µm plankton net in the shallow Ria de Aveiro estuary (western Portugal). The wide variety of harpacticoid forms exploits different and particular types of habitats (sediment, phytal and planktonic), which require specialized features (Bell et al., Reference Bell, Walters and Hall1987; Boxshall & Halsey, Reference Boxshall and Halsey2004; Suárez-Morales et al., Reference Suárez-Morales, De Troch and Fiers2006). In some cases, these copepods are associated with other organisms (e.g. polychaeta) since they can benefit from the fact that: (1) the harpacticoids are less subjected to predation or disturbance, since the structure confer a source of predation refuge; and (2) the organism (the structure builder) may stimulate microbial growth providing food availability (Thistle & Eckman, Reference Thistle and Eckman1988). Accordingly, species exhibit a variety of morphological characteristics and may be found migrating from different habitats. Different forms may still be represented in the Mondego estuary fauna.
Our study is a first attempt to give an overview of the harpacticoid species present in the Mondego estuary, a temperate shallow estuarine system from southern Europe. A next step forward could be to analyse the function of these harpacticoids in the system. Since harpacticoid copepods form an important link between primary production and higher trophic levels (De Troch et al., Reference De Troch, Mees and Wakwabi1998, Reference De Troch, Vandepitte, Raes, Suárez-Morales and Vincx2005; Buffan-Dubau & Carman, Reference Buffan-Dubau and Carman2000), unravelling their role in Mondego estuary will be an essential contribution to understand the functioning of ecosystems and the effects of potential threats.
ACKNOWLEDGEMENTS
The Portuguese Foundation for Science and Technology (FCT, Portugal) financed Ana M.M. Gonçalves (SFRH/BD/30475/2006) by means of individual research grants. Ana Gonçalves also acknowledges FCT for their financial support to develop this work in UGent, Belgium. The second author is a Postdoctoral Fellow of the Research Foundation–Flanders (FWO). Ana Gonçalves acknowledges Dr F. Fiers (KBIN, Belgium) and Dr H. Gheerardyn (UGent, Belgium) for their support in Harpacticoida identification.
